METHIONINE ADENOSYLTRANSFERASE4 Mediates DNA and Histone Methylation

Meng, Jingjing; Wang, Lishuan; Wang, Jingyi; Zhao, Xue; Cheng, Jinkui; Yu, Wenbo; Jin, Dan; Li, Qing; Gong, Zhizhong

doi:10.1104/pp.18.00183

Cited by 58 publications

(55 citation statements)

References 73 publications

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“…The status of cellular metabolism is closely connected to epigenetic modifications (59,60). Nutrition is well known to affect development and diseases through metabolism that modulates epigenetic modifications in mammals (61).…”

Section: Discussionmentioning

confidence: 99%

Peroxisomal β-oxidation regulates histone acetylation and DNA methylation in Arabidopsis

Wang

Liu

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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Epigenetic markers, such as histone acetylation and DNA methylation, determine chromatin organization. In eukaryotic cells, metabolites from organelles or the cytosol affect epigenetic modifications. However, the relationships between metabolites and epigenetic modifications are not well understood in plants. We found that peroxisomal acyl-CoA oxidase 4 (ACX4), an enzyme in the fatty acid β-oxidation pathway, is required for suppressing the silencing of some endogenous loci, as well as Pro35S:NPTII in the ProRD29A:LUC/C24 transgenic line. The acx4 mutation reduces nuclear histone acetylation and increases DNA methylation at the NOS terminator of Pro35S:NPTII and at some endogenous genomic loci, which are also targeted by the demethylation enzyme REPRESSOR OF SILENCING 1 (ROS1). Furthermore, mutations in multifunctional protein 2 (MFP2) and 3-ketoacyl-CoA thiolase-2 (KAT2/PED1/PKT3), two enzymes in the last two steps of the β-oxidation pathway, lead to similar patterns of DNA hypermethylation as in acx4. Thus, metabolites from fatty acid β-oxidation in peroxisomes are closely linked to nuclear epigenetic modifications, which may affect diverse cellular processes in plants.H istone acetylation is important for neutralizing the positive charges of lysine residues and promoting chromatin relaxation; it is also required for transcription, DNA replication, histone methylation, and other histone modifications (1-4). Histones are acetylated by acetyltransferases, which transfer acetyl groups from acetyl-CoA to histone lysine residues.Acetyl-CoA is a central metabolite that can be produced via several metabolic pathways involved in pyruvate, citrate, acetate, and fatty acid β-oxidation metabolism (5). In mammals, acetyl-CoA in mitochondria is produced from different pathways, including the fatty acid β-oxidation (6). In cytosol and nucleus, adenosine triphosphate (ATP)-citrate lyase (ACLY) cleaves citrate exported from mitochondria to regenerate acetyl-CoA that can be used for other biosynthetic processes, such as fatty acid synthesis and histone acetylation (6). In mouse, conditional loss of carnitine palmitoyltransferase 1A (CPT1A), which is required for the transfer of fatty acid into mitochondria for β-oxidation, impairs dermal lymphatic formation via histone acetylation in an ACLY-dependent manner (7). A pyruvate dehydrogenase complex can be translocated from mitochondria to nuclei to generate acetyl-CoA and mediate histone acetylation in mammalian cells in certain conditions (2,8). In Arabidopsis, the mutations in cytosolic acetyl-CoA carboxylase (ACC1), which converts cytosolic acetyl-CoA to malonyl-CoA for elongating the plastid-produced fatty acids, lead to high accumulation of cytosolic acetyl-CoA, specifically resulting in increased H3K27 acetylation (H3K27ac) (9).These results underscore the importance of acetyl-CoA in histone acetylation in nuclei in both mammals and plants. However, in plant cells, plastids, mitochondria, peroxisomes, and cytosol can produce acetyl-CoA (10). Whether impairment of metabolism ...

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Section: Discussionmentioning

confidence: 99%

Peroxisomal β-oxidation regulates histone acetylation and DNA methylation in Arabidopsis

Wang

Liu

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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“…To investigate the inhibitory effect of SAM and Ile on kinase autophosphorylation in the greening process, WT, sty8 sty46, sty46/ 35 S::STY46, and sty8 sty46/ 35 S::STY46⌬ACT lines were analyzed on MS plates supplemented with 8 M SAM and 100 M Ile (18,19) (Fig. 5D).…”

Section: Impact Of Deletion Of the Act Domain In Plantamentioning

confidence: 99%

The ACT domain in chloroplast precursor–phosphorylating STY kinases binds metabolites and allosterically regulates kinase activity

Eisa

Bölter

Schwenkert

2019

Journal of Biological Chemistry

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Protein import of nucleus-encoded proteins into plant chloroplasts is a highly regulated process, requiring fine-tuning mechanisms especially during chloroplast differentiation. One way of altering import efficiency is phosphorylation of chloroplast transit peptides in the cytosol. We recently investigated the role of three serine/threonine/tyrosine (STY) kinases, STY8, STY17, and STY46, in precursor phosphorylation. These three kinases have a high degree of similarity and harbor a conserved aspartate kinase–chorismate mutase–tyrA (prephenate dehydrogenase) (ACT) domain upstream of the kinase domain. The ACT domain is a widely distributed structural motif known to be important for allosteric regulation of many enzymes. In this work, using biochemical and biophysical techniques in vitro and in planta, including kinase assays, microscale thermophoresis, size exclusion chromatography, as well as site-directed mutagenesis approaches, we show that the ACT domain regulates autophosphorylation and substrate phosphorylation of the STY kinases. We found that isoleucine and S-adenosylmethionine bind to the ACT domain, negatively influencing its autophosphorylation ability. Moreover, we investigated the role of the ACT domain in planta and confirmed its involvement in chloroplast differentiation in vivo. Our results provide detailed insights into the regulation of enzyme activity by ACT domains and establish that it has a role in binding amino acid ligands during chloroplast biogenesis.

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“…For example, hydroxycinnamoyl-CoA: shikimate hydroxycinnamoyl transferase (spot 1603; HCT, AT5G48930) is related to the accumulation of flavonoids and in turn represses auxin transport to inhibit plant growth (Li et al, 2010). Methionine adenosyltransferase 4 (spot 3529; MAT4, AT3G17390) plays an important role in S -adenosyl-Met (SAM) production and plant development (Meng et al, 2018). β-Ketoacyl-[acyl carrier protein] synthase I (spot 1504; KASI, AT5G46290) is important for fatty acid synthesis and plays a key role in embryo development and chloroplast division (Wu and Xue, 2010).…”

Section: Resultsmentioning

confidence: 99%

Transcriptomic and Proteomic Analysis of Shaan2A Cytoplasmic Male Sterility and Its Maintainer Line in Brassica napus

Ning

Wang

et al. 2019

Front. Plant Sci.

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Cytoplasmic male sterility (CMS) lines are widely used for hybrid production in Brassica napus . The Shaan2A CMS system is one of the most important in China and has been used for decades; however, the male sterility mechanism underlying Shaan2A CMS remains unknown. Here, we performed transcriptomic and proteomic analysis, combined with additional morphological observation, in the Shaan2A CMS. Sporogenous cells, endothecium, middle layer, and tapetum could not be clearly distinguished in Shaan2A anthers. Furthermore, Shaan2A anther chloroplasts contained fewer starch grains than those in Shaan2B (a near-isogenic line of Shaan2A), and the lamella structure of chloroplasts in Shaan2A anther wall cells was obviously aberrant. Transcriptomic analysis revealed differentially expressed genes (DEGs) mainly related to carbon metabolism, lipid and flavonoid metabolism, and the mitochondrial electron transport/ATP synthesis pathway. Proteomic results showed that differentially expressed proteins were mainly associated with carbohydrate metabolism, energy metabolism, and genetic information processing pathways. Importantly, nine gene ontology categories associated with anther and pollen development were enriched among down-regulated DEGs at the young bud (YB) stage, including microsporogenesis, sporopollenin biosynthetic process, and tapetal layer development. Additionally, 464 down-regulated transcription factor (TF) genes were identified at the YB stage, including some related to early anther differentiation such as SPOROCYTELESS ( SPL , also named NOZZLE , NZZ ), DYSFUNCTIONAL TAPETUM 1 ( DYT1 ), MYB80 (formerly named MYB103 ), and ABORTED MICROSPORES ( AMS ). These results suggested that the sterility gene in the Shaan2A mitochondrion might suppress expression of these TF genes in the nucleus, affecting early anther development. Finally, we constructed an interaction network of candidate proteins based on integrative analysis. The present study provides new insights into the molecular mechanism of Shaan2A CMS in B. napus .

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METHIONINE ADENOSYLTRANSFERASE4 Mediates DNA and Histone Methylation

Cited by 58 publications

References 73 publications

Peroxisomal β-oxidation regulates histone acetylation and DNA methylation in Arabidopsis

Peroxisomal β-oxidation regulates histone acetylation and DNA methylation in Arabidopsis

The ACT domain in chloroplast precursor–phosphorylating STY kinases binds metabolites and allosterically regulates kinase activity

Transcriptomic and Proteomic Analysis of Shaan2A Cytoplasmic Male Sterility and Its Maintainer Line in Brassica napus

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